Foliar oxidative stress and insect herbivory

Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance

J. L. Bi, Gary Felton

Research output: Contribution to journalArticle

220 Citations (Scopus)

Abstract

Oxidative responses of plants to pathogens and other environmental stresses have received considerable recent attention. We propose that an oxidative response also occurs following attack by herbivores. Our data strongly indicate a shift in the oxidative status of soybean following herbivory by the insect Helicoverpa zea. Herbivory caused significant increases in lipid peroxidation and ·OH radical formation. The activity of several oxidative enzymes including lipoxygenases, peroxidase, diamine oxidase, ascorbate oxidase, and NADH oxidase I increased after herbivory on soybean. The enhanced production of phenolic compounds is indicated by an increase in the activity of phenylalanine ammonia lyase in wounded tissues. On the other hand, the level of soybean foliar antioxidants such as ascorbic acid, total carotenoids, nonprotein thiols, and catalase decreased significantly following herbivory. These results implicate primary compounds (e.g., ascorbic acid, proteins), secondary metabolites (e.g., phenolics), and reactive oxygen species (e.g., hydroxyl radical, hydrogen peroxide) as multiple components of induced resistance. The oxidative changes in the host plant correspond with increased oxidative damage in the midgut of insects feeding on previously wounded plants. Decreases in nonprotein thiols and reduced ascorbic acid occurred in midgut epithelial tissue from insects feeding on wounded plants compared to the insects on control plants. In contrast, midgut hydroperoxides and dehydroascorbic acid concentrations were greater in insects on wounded plants compared to their counterparts on control plants. We conclude that oxidative responses in soybean may have both positive and negative effects upon the host plant: a decrease in herbivory and an increase in oxidative damage to the plant. The salient benefit to the plant, in terms of insect resistance, is the relative balance between these opposing effects.

Original languageEnglish (US)
Pages (from-to)1511-1530
Number of pages20
JournalJournal of Chemical Ecology
Volume21
Issue number10
DOIs
StatePublished - Oct 1 1995

Fingerprint

Herbivory
Oxidative stress
induced resistance
secondary metabolite
Metabolites
herbivory
secondary metabolites
Ascorbic Acid
Insects
reactive oxygen species
Reactive Oxygen Species
Oxidative Stress
oxidative stress
herbivores
insect
Sulfhydryl Compounds
Hydrogen Peroxide
insects
Ascorbate Oxidase
Lipoxygenases

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Biochemistry

Cite this

@article{c33a645d4c9b4286be3a2def1f299365,
title = "Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance",
abstract = "Oxidative responses of plants to pathogens and other environmental stresses have received considerable recent attention. We propose that an oxidative response also occurs following attack by herbivores. Our data strongly indicate a shift in the oxidative status of soybean following herbivory by the insect Helicoverpa zea. Herbivory caused significant increases in lipid peroxidation and ·OH radical formation. The activity of several oxidative enzymes including lipoxygenases, peroxidase, diamine oxidase, ascorbate oxidase, and NADH oxidase I increased after herbivory on soybean. The enhanced production of phenolic compounds is indicated by an increase in the activity of phenylalanine ammonia lyase in wounded tissues. On the other hand, the level of soybean foliar antioxidants such as ascorbic acid, total carotenoids, nonprotein thiols, and catalase decreased significantly following herbivory. These results implicate primary compounds (e.g., ascorbic acid, proteins), secondary metabolites (e.g., phenolics), and reactive oxygen species (e.g., hydroxyl radical, hydrogen peroxide) as multiple components of induced resistance. The oxidative changes in the host plant correspond with increased oxidative damage in the midgut of insects feeding on previously wounded plants. Decreases in nonprotein thiols and reduced ascorbic acid occurred in midgut epithelial tissue from insects feeding on wounded plants compared to the insects on control plants. In contrast, midgut hydroperoxides and dehydroascorbic acid concentrations were greater in insects on wounded plants compared to their counterparts on control plants. We conclude that oxidative responses in soybean may have both positive and negative effects upon the host plant: a decrease in herbivory and an increase in oxidative damage to the plant. The salient benefit to the plant, in terms of insect resistance, is the relative balance between these opposing effects.",
author = "Bi, {J. L.} and Gary Felton",
year = "1995",
month = "10",
day = "1",
doi = "10.1007/BF02035149",
language = "English (US)",
volume = "21",
pages = "1511--1530",
journal = "Journal of Chemical Ecology",
issn = "0098-0331",
publisher = "Springer New York",
number = "10",

}

TY - JOUR

T1 - Foliar oxidative stress and insect herbivory

T2 - Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance

AU - Bi, J. L.

AU - Felton, Gary

PY - 1995/10/1

Y1 - 1995/10/1

N2 - Oxidative responses of plants to pathogens and other environmental stresses have received considerable recent attention. We propose that an oxidative response also occurs following attack by herbivores. Our data strongly indicate a shift in the oxidative status of soybean following herbivory by the insect Helicoverpa zea. Herbivory caused significant increases in lipid peroxidation and ·OH radical formation. The activity of several oxidative enzymes including lipoxygenases, peroxidase, diamine oxidase, ascorbate oxidase, and NADH oxidase I increased after herbivory on soybean. The enhanced production of phenolic compounds is indicated by an increase in the activity of phenylalanine ammonia lyase in wounded tissues. On the other hand, the level of soybean foliar antioxidants such as ascorbic acid, total carotenoids, nonprotein thiols, and catalase decreased significantly following herbivory. These results implicate primary compounds (e.g., ascorbic acid, proteins), secondary metabolites (e.g., phenolics), and reactive oxygen species (e.g., hydroxyl radical, hydrogen peroxide) as multiple components of induced resistance. The oxidative changes in the host plant correspond with increased oxidative damage in the midgut of insects feeding on previously wounded plants. Decreases in nonprotein thiols and reduced ascorbic acid occurred in midgut epithelial tissue from insects feeding on wounded plants compared to the insects on control plants. In contrast, midgut hydroperoxides and dehydroascorbic acid concentrations were greater in insects on wounded plants compared to their counterparts on control plants. We conclude that oxidative responses in soybean may have both positive and negative effects upon the host plant: a decrease in herbivory and an increase in oxidative damage to the plant. The salient benefit to the plant, in terms of insect resistance, is the relative balance between these opposing effects.

AB - Oxidative responses of plants to pathogens and other environmental stresses have received considerable recent attention. We propose that an oxidative response also occurs following attack by herbivores. Our data strongly indicate a shift in the oxidative status of soybean following herbivory by the insect Helicoverpa zea. Herbivory caused significant increases in lipid peroxidation and ·OH radical formation. The activity of several oxidative enzymes including lipoxygenases, peroxidase, diamine oxidase, ascorbate oxidase, and NADH oxidase I increased after herbivory on soybean. The enhanced production of phenolic compounds is indicated by an increase in the activity of phenylalanine ammonia lyase in wounded tissues. On the other hand, the level of soybean foliar antioxidants such as ascorbic acid, total carotenoids, nonprotein thiols, and catalase decreased significantly following herbivory. These results implicate primary compounds (e.g., ascorbic acid, proteins), secondary metabolites (e.g., phenolics), and reactive oxygen species (e.g., hydroxyl radical, hydrogen peroxide) as multiple components of induced resistance. The oxidative changes in the host plant correspond with increased oxidative damage in the midgut of insects feeding on previously wounded plants. Decreases in nonprotein thiols and reduced ascorbic acid occurred in midgut epithelial tissue from insects feeding on wounded plants compared to the insects on control plants. In contrast, midgut hydroperoxides and dehydroascorbic acid concentrations were greater in insects on wounded plants compared to their counterparts on control plants. We conclude that oxidative responses in soybean may have both positive and negative effects upon the host plant: a decrease in herbivory and an increase in oxidative damage to the plant. The salient benefit to the plant, in terms of insect resistance, is the relative balance between these opposing effects.

UR - http://www.scopus.com/inward/record.url?scp=0029189303&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0029189303&partnerID=8YFLogxK

U2 - 10.1007/BF02035149

DO - 10.1007/BF02035149

M3 - Article

VL - 21

SP - 1511

EP - 1530

JO - Journal of Chemical Ecology

JF - Journal of Chemical Ecology

SN - 0098-0331

IS - 10

ER -